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Evo Edu Outreach (2008) 1:439–447
DOI 10.1007/s12052-008-0084-1
ORIGINAL SCIENTIFIC ARTICLE
Charting Evolution’s Trajectory: Using Molluscan Eye
Diversity to Understand Parallel and Convergent Evolution
Jeanne M. Serb & Douglas J. Eernisse
Published online: 25 September 2008
# Springer Science + Business Media, LLC 2008
Abstract For over 100 years, molluscan eyes have been
used as an example of convergent evolution and, more
recently, as a textbook example of stepwise evolution of a
complex lens eye via natural selection. Yet, little is known
about the underlying mechanisms that create the eye and
generate different morphologies. Assessing molluscan eye
diversity and understanding how this diversity came about
will be important to developing meaningful interpretations
of evolutionary processes. This paper provides an introduction to the myriad of eye types found in molluscs, focusing
on some of the more unusual structures. We discuss how
molluscan eyes can be applied to the study of evolution by
examining patterns of convergent and parallel evolution and
provide several examples, including the putative convergence
of the camera-type eyes of cephalopods and vertebrates.
Keywords Mollusca . Eye . Pax6 . Camera-type eye .
Evolution . Convergent evolution . Parallel evolution
The Mollusca is a large animal phylum, second only to the
Arthropoda in the number of described living species. An
estimated 100,000 species are distributed among seven
classes: Aplacophora, Polyplacophora, Monoplacophora,
Scaphopoda, Gastropoda, Cephalopoda, and Bivalvia
(Ruppert et al. 2004). Each class is recognized by
alternations to a basic molluscan body plan. For example,
the arms and tentacles of a squid are a modification of the
J. M. Serb (*)
Department of Ecology, Evolution and Organismal Biology,
Iowa State University,
253 Bessey Hall,
Ames, IA 50011, USA
e-mail: [email protected]
D. J. Eernisse
Department of Biological Science, California State University,
Fullerton, CA 92834, USA
muscular foot common in other molluscan lineages. The
largest classes by far are Gastropoda (snails, slugs; 60,000
species) and Bivalvia (clams, oysters, mussels; 10,000
species). Polyplacophora (chitons) and Cephalopoda (squids,
octopuses) are smaller classes, each containing nearly 1,000
species. Of the seven molluscan classes, it is these four classes
that possess eyes.
Molluscan eyes are extremely varied, ranging from a
simple eye cup or pit eye that is open to the environment to
closed lens eyes much like those seen in fish (Fig. 1),
compound eyes that superficially resemble the eyes of flies,
pinhole eyes, and eyes with mirrors. In fact, molluscs have
some of the greatest morphological diversity of eye types
among all animals, with seven to 11 different lineages
possessing eyes (von Salvini-Plawen and Mayr 1977). The
size of molluscan eyes ranges from less than 0.02 mm
(0.00078 in.) across in the diminutive small spot snail,
Punctum minutissimum (Timothy Pearce, Carnegie Museum
of Natural History, personal communication), to more than
27 cm (11 in.) across in the colossal squid (Mesonychoteuthis
hamiltoni), about 11 times the size of a human eye (Black
2008; Lilley 2008).
In addition to the incredible diversity of eye structures
and size range, the placement of eyes varies across
molluscan taxa. Two of the four classes, gastropods and
cephalopods, have a well-developed head (cephalic) region,
so only they can have cephalic eyes, and most of them do,
whereas Bivalvia and Polyplacophora have many replicated
eyes in other parts of the body, such as along the ventral
edge of the mantle or within a shell. Although many
molluscan species possess light-sensitive structures, such as
nerve endings in their epidermis as adults, and eye spots, a
composite of light-sensitive and pigment cells as larvae,
that are functionally important to the organism, we do not
consider these to be true eyes. Instead, we define eyes as
organs that can sense both light intensity and direction with
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a
PC
ON
OC
RC
b
RC
CO
ON
L
PC
Fig. 1 Schematic drawing of two common eye types found in
molluscs. An open pit eye in a does not have a lens or cornea and is
open to the environment through an opening in the optical cup (OC).
The closed lens eye in b has both a lens (L) and a cornea (CO). Both
eyes have optic nerves (ON), photoreceptor cells (RC), and pigment
cells (PC)
the necessary components for at least rudimentary spatial
resolution or image-forming capabilities.
What Makes an Eye?
At its most basic construction, an eye must have lightsensitive photoreceptor cells arranged in a cup shape and
surrounded by pigment cells so that light from the
environment can only hit a photoreceptor cell from one
direction (Land and Nilsson 2002). Furthermore, a true eye
can register light information from multiple photoreceptors
simultaneously, and this information can be processed in
parallel by the organism. Generally, the photoreceptor cells
are arranged in a single layer to form a retina. These
photoreceptor cells can be one of two types, identified by
different ways of increasing cell surface area. If they have
expansions on the ciliary membrane, they are ciliary
photoreceptors, while rhabdomeric photoreceptors have
extensions on the cell membrane as villi (Eakin 1979).
Additional eye structures that are present in some eye types
include a cellular or secreted cornea, lenses, vitreous
masses, and reflective surfaces.
How well does an organism “see?” The functional
performance of an eye is measured by its spatial resolution
(the quality of the image) and by its sensitivity (ability to
get enough light to the photoreceptors so that resolution is
maximized; Land Nilsson 2002). Spatial resolution is
determined by the spacing of the photoreceptors along the
retina. In general, closer-packed photoreceptors provide a
clearer image. Thus, the visual capabilities of organisms
can be compared by calculating the resolving power of their
eyes. Like other aspects of molluscan eyes, spatial
resolution varies greatly among species (Table 1). For
example, the resolution of gastropod eyes broadly overlaps
with both vertebrate and arthropod eyes.
This paper provides an introduction to the myriad of eye
types found in molluscs, highlighting some of the more
unusual structures. We discuss how molluscan eyes can be
applied to the study of evolution by examining patterns of
convergent and parallel evolution and provide several
examples, such as the putative convergence of the cameratype eyes of cephalopods and vertebrates and the similarity
of compound eyes in the ark clams and arthropods.
The Chitons (Polyplacophora) and Their Simple
Photoreceptors
The polyplacophorans (chitons) are multi-shelled marine
molluscs often found attached to rocks on the seashore.
Chitons respond to a bright directional light by moving
away from it (Omelich 1967; Boyle 1972). In general,
chitons tend to seek refuge under a rock during the day and
emerge to forage at night, probably to avoid potential
predators. They are also wary of shadows, for example, one
that might be cast by a hungry bird. Their “shadow
response” can be sudden. Crozier and Arey (1918)
observed that a shadow of a fly 2 m away caused Chiton
tuberculatus to stop temporarily in its trek across a rock.
How does a chiton respond so quickly to a bright light or a
shadow? Chitons (like most molluscs except the familiar
cephalopods and gastropods) not only lack cephalic eyes
but they also lack a head. They also lack a central nervous
system and barely even have ganglionic swellings along
their ladder-like nervous system. Chitons are the only
molluscs to have a living outer layer of their calcium
carbonate shell, and their primary sensory organs are either
arranged in neat rows or more randomly scattered across
the upper surface of their multiple shell plates (Blumrich
1891; reviewed by Fischer 1988; Eernisse and Reynolds
1994; Reindl et al. 1997; Schwabe and Wanninger 2006;
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Table 1 Spatial resolution of a
selection of animal eyes
a
Based on acceptance
angle Δρ
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Name
Resolution/inter-receptor angle (Δ, °)
Eagle
Human
Octopus (cephalopod)
Cat
Strombus luhuanus (gastropod)
Honeybee
Planorbaruis corneus (gastropod)
Scallop (Pecten maximus, bivalve)
Lymnaea stagnalis (gastropod)
Littorina littorea (gastropod)
Fruit fly
Nautilus (cephalopod)
Cepaea nemorais (gastropod)
Trichia hispida (gastropod)
Helix aspersa (gastropod)
Giant clam (Tridacna maxima, bivalve)
Ark clam (Barbatia cancellaria, bivalve)
Planaria (flatworm)
0.0036
0.007
0.011
0.05
0.23
0.95
1.4
1.6
2.5
4.5
5.0
8.0
8.0
13.0
14.5
20.0
32.0
35.0
Vendrasco et al. 2008). These sensory organs (termed
aesthetes or esthetes) have been demonstrated experimentally to be capable of photoreception, and in at least some
chitons, they probably have other sensory capabilities as
well. Much remains unknown about how chitons see their
world, but it is likely that most chitons are capable of
responding to light in an adaptive manner. It is possible that
their often thousands of spaced aesthetes, in addition to
similar organs in the soft tissues surrounding their shells,
provide the entire exposed surface of the animal with a sort
of giant compound eye, allowing a coordinated response.
Chitons have a long fossil record, and aesthetes are well
known from some of the oldest fossil shell plates of chitons
that lived over 400 million years ago (e.g., Vendrasco et al.
2004). Modern chitons typically have spaced macroaesthetes, each surrounded by multiple microaesthetes, and
their similar appearance in ancient relatives implies that
their function has long been important and conserved. All
modern chitons have aesthetes, with or without added
pigmentation. Two particular lineages of chitons have not
only aesthetes but also much larger and complex sensory
organ called an ocellus (Fig. 2a–c; Moseley 1885; Nowikoff
1907). The ocellus has a lens, a vitreous area, and a cup of
retinal cells with microvillous rhabdomes (Boyle 1969);
these provide all the components necessary for spatial vision.
Ocelli are large enough to be seen with a naked human eye
(unlike aesthetes), but they are most likely too small to form
images on a retina. The ocelli are highly repetitive structures
where a single individual of Onithochiton neglectus can have
411 to 1,472 ocelli in rows along all shell valves (Boyle
1969). Why have so many ocelli if they function similarly to
the simple aesthetes? Both chiton species with or without
ocelli are usually, but not always, nocturnal. Further, it ap-
(Land and Nilsson 2002)
(Land and Nilsson 2002)
(Land and Nilsson 2002)
(Land and Nilsson 2002)
(Land 1981)
(Land and Nilsson 2002)
(Zieger and Meyer-Rochow 2008)
(Land and Nilsson 2002)
(Zieger and Meyer-Rochow 2008)
(Land and Nilsson 2002)
(Land and Nilsson 2002)
(Land and Nilsson 2002)
(Zieger and Meyer-Rochow 2008)
(Zieger and Meyer-Rochow 2008)
(Hamilton and Winter 1982)
(Land 2003)
(Nilsson 1994)a
(Land and Nilsson 2002)
pears that most species will respond to low intensities of
light, including moonlight, even if the individual lacks ocelli
(Omelich 1967). Therefore, it remains a mystery what
additional functions the ocelli might provide to those chitons
with them.
Because fossil chitons with ocelli are younger than ten
million years, it is likely that ocelli are among the most
recently evolved of all animal eyes. Perhaps their study can
provide insight into how an eye might evolve. By
comparing across the species of chitons with ocelli and
their nearest relatives, there is an opportunity to investigate
stages in the transition between simple photoreceptors to
meditate light response behavior and true eyes.
More Complex (and More Kinds) of Eyes: The Bivalves
Bivalves (clams, mussels, oysters) are laterally compressed
organisms typically adapted for life within the sediment of
marine and freshwater systems. In general, these headless
animals are relatively immobile as adults, and when sensory
organs, including the eyes, are present, they are found on
exposed tissues. It is thought that bivalve eyes are primarily
used to detect predators and elicit a defense response,
creating a type of optical “burglar alarm” for the animal
(Nilsson 1994). Many bivalves possess eyes along the
ventral margin of their mantle, which lines the shell. These
are called pallial eyes, in reference to a mantle or cloak (Gk.
pallium; Fig. 2d). In some taxa (e.g., Cerastoderma edule),
pallial eyes are associated with siphons used for respiration
and filter feeding (Morton 2001) and are often the only part
of the bivalve not buried within the substrate. Pallial eyes
are highly repetitive structures numbering in the tens
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Fig. 2 Diversity of eye types in
four molluscan classes.
a Dorsal view of the shell plates
and ocelli of a chiton
(Polyplacophora: Tonicia
lebruni). b, c Magnified views
of ocelli on the anterior shell
plate. d Highly repetitive pallial
eyes along the mantle edge
of the scallop (Bivalvia:
Argopecten irradians).
e Cephalic eyes (Gastropoda:
Strombus). f Camera-type eyes
in the squid (Cephalopoda:
Loligo). g Cuttlefish
(Cephalopoda: Sepia). Images
are copyrighted and used with
permission by the following:
a–c A. Draeger and D. Eernisse,
d W. Capman, e H. Chaney, and
f–g L. J. Friesen
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a
b
c
d
e
© W. Capman
© H. Chaney
f
g
© L. J. Friesen
(Barber and Land 1967) to thousands (Wilkens 1986) per
individual. Structurally, pallial eyes in bivalves are more
diverse than cephalic eyes in other taxa. Pallial eyes can be
either open pit or closed lens eyes (Fig. 1a,b), and some
species may have several eye types along the mantle edge
(e.g., Barbatia cancellaria). Some pallial eyes can have
© L. J. Friesen
accessory organs that connect to the optic nerve and are
adjacent to each eye (e.g., Cerastoderma edule, Tridacna
maxima). Others may have single or double layers of
photoreceptor cells, each composed of a different photoreceptor cell type (ciliary vs. rhabdomeric; e.g., Pectinidae,
Laternulidae). In the giant clam, Tridacna maxima, pallial
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eyes not only sense the visual world (Wilkens 1988; Land
2003) but may also direct light to photo-symbionts living
within the mantle tissue of the host (Fankboner 1981).
Two of the most complex and unusual eye types in
bivalves are in the ark clams (Arcoida) and the scallops
(Pectinidae). Two eye types are found in the ark clams, a
simple cup eye and a multifaceted compound eye (Nilsson
1994; Patten 1887; Waller 1980). The compound eye is
similar to the structure of the arthropod compound eye but
is evolutionarily independent (Nilsson and Kelber 2007).
An individual clam can have 200–300 compound eyes
along the mantle edge. Current research suggests that the
large number of eyes found in the ark clams are used to
detect motion rather than form images of the environment
(Nilsson 1994). The numerous eyes provide a more
complete visual coverage of the bivalve’s environment
and better sensitivity to visual signals (Nilsson 1994).
The blue eyes of the scallop are among the best-known
molluscan eyes (Fig. 2d). These eyes are lined with a sheet
of guanine crystals that creates a concave mirror in the back
of the eye. It is this mirror that forms an image of the
environment by a reflection from the back of the eye onto a
double retina directly behind the lens (Land 1965, 1984).
Each retina is composed of different photoreceptor cells,
ciliary photoreceptors in the distal retina, and rhabdomeric
photoreceptors in the proximal retina. Experimental work
on behavior and physiology has demonstrated that scallops
respond to the distribution and intensity of light and can
detect moving objects (von Buddenbrock and Moller-Racke
1953). There is also evidence that scallops use visual cues
to discriminate between environments and to direct their
swimming (Hamilton and Koch 1996) or adjust feeding
behavior relative to the size of particles they see suspended
in the water (Speiser and Johnsen 2008).
Expanding Eye Diversity: The Gastropods
Gastropods (snails, slugs) have a wide variety of eye types
ranging from simple pit eyes without lenses or corneas to
complex lens eyes (see reviews in Messenger 1981; Charles
1966; Chase 2002; Bobkova et al. 2004; Zieger and MeyerRochow 2008). Most gastropods have a pair of cephalic
eyes which can be at the base of cephalic tentacles, on the
tips of retractable tentacles so that the eye can be withdrawn
into the tentacle, or on short stalks (Fig. 2e).
In addition to cephalic eyes, there are several unique
sensory structures in the gastropods. Some pulmonate
gastropod lineages, such as the terrestrial slugs (e.g.,
Limacidae), possess a double eye. This is a ventral
extension of the retina composed of photoreceptor cells
and un-pigmented supporting cells. When a lens is on this
structure, it is treated as a second “eye” (Tamamaki 1989),
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while a lensless extension is called an “accessory retina”
(Henchman 1897; description in Zieger and Meyer-Rochow
2008). It has been hypothesized that this structure may be
involved in infrared detection (Newell and Newell 1968),
but this has not been physiologically verified. Others have
suggested that the two retinas of the double eye are used
under different light intensities, thus expanding visual
capability of the organism in a range of light conditions
(see discussion in Kataoka 1977). Further research is
needed to better understand the function of the double eye.
In some species of marine slugs (Onchidium), individual
animals possess two eye types. The first type is a pair of
cephalic eyes structurally similar to other lens eyes of
gastropods (Katagiri et al. 1995). The second eye type is a
lens eye that projects from the back of the animal (Hirasaka
1922). Each of the dorsal eyes is an open vesicle, spherical
in shape, with a cup-shaped pigment layer, a ciliary-based
retina, and lens, but lacks a cornea. These eyes appear to
have image-forming capabilities and may create a “reasonable image” (Arey and Crozier 1921; Land 1968). See
detailed descriptions of both eye types in Katagiri et al.
(2002) and references therein.
Probably the most sophisticated and unique eye in the
gastropods is the much-elongated “telescopic” eye of
pelagic heteropods. These mobile carnivores spend their
entire life cycle in the water column and possess many
adaptations to this lifestyle, including a reduction or loss of
shell, the modification of the muscular foot into a fin, and
development of perhaps the most efficient gastropod eye
(reviewed by Lalli and Gilmer 1989). Unlike the typical
gastropod retina, the heteropod retina does not form a cup;
rather, it is a long strip of three to six cells in width,
resulting in a very narrow field of view. These eyes move in
a systematic scanning motion, which may be used to
detect prey (see Land 1982 for description). Even the
composition of the heteropod retina is unusual and may
contain several photoreceptor types that are unlike ciliary or
rhabdomeric receptors found in cephalic eyes of other
molluscs (Land 1984).
Specialized Eyes: The Cephalopods
Cephalopods (nautilus, squid, octopus) are a lineage of
highly specialized predators. More than any other mollusc
group, cephalopods rely on vision for prey capture, predator
avoidance, and communication (Budelmann 1996; Hanlon
and Messenger 1996; Muntz 1999; Hanlon 2007). Therefore, it is no surprise that these animals possess eyes with
excellent perception and visual acuity (Messenger 1981).
There are two well-known cephalopod eye types. The
pinhole eye type is only found in pearly nautiluses
(Nautilidae), recognized by their chambered shell. The
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nautiloids and the similar but long-extinct ammonoids were
once dominant predators in ancient seas, yet their eyes are
only known from the six surviving species of pearly
nautiluses. The nautilus eye is unusual, as it is a chamber
open to the environment and does not have a cornea or lens
to focus light. Instead, these eyes appear to function like a
pinhole camera (Hurley et al. 1978; Messenger 1981). In
nautiloids, the iris forms a small adjustable opening (pupil).
The light rays reflected off an object pass through the pupil
and form an inverted image of the object on the retina at the
back of the eye. All other living cephalopods belong to the
coleoid (internal shelled) cephalopods and possess a
camera-type eye (Fig. 2f,g). This eye optically functions
in a manner similar to the vertebrate eye, making the
cephalopod eye a putative example of convergent evolution
(Packard 1972). The cephalopod eye resembles the all-rod
eye seen in sharks, with similar optics, speed, sensitivity,
and resolution (Packard 1972). Morphological similarities
of the eyes include an iris, nearly circular lens, vitreous
cavity, and photoreceptor cells that form the retina;
however, the photoreceptors in the cephalopod eye are
rhabdomeric, not ciliary as in vertebrate eyes (Young 1962).
Structurally, the cephalopod eye differs from the vertebrate eye. Cephalopods do not have a cornea, and the retina
is everted so that the distal end of photoreceptive cells lies
directly behind the lens and points toward incoming light.
As a result, photoreceptor cells connect to the optic nerve
behind the retina (Packard 1972). In the vertebrate eye,
photoreceptive cells are behind transparent ganglion cells,
reversing the orientation of the retina and creating a “blind
spot,” an area devoid of photoreceptor cells where the optic
nerve passes through it (Nicol 1989). This means that
unlike vertebrates, there is no “blind spot” in the cephalopod
eye. Similarities and differences in morphology and development of the coleolid cephalopod eye and the fish eye have
been reviewed extensively elsewhere (Packard 1972;
Messenger 1981; Yamamoto 1985; Harris 1997; Land
and Nilsson 2002).
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unrelated or distantly related lineages. In other words, two
lineages have evolved convergently if they started from
different ancestral morphologies and evolved towards the
same (adaptive) phenotype (Fig. 3a). For example, the
wings in animals, such as birds, bats, and pterosaurs—an
extinct group of flying reptiles—are convergent. These
animals belong to different families and are distantly related
(i.e., do not share a common ancestor). However, they
arrive at similar phenotypic endpoints because the same
laws of aerodynamics apply to determine wing shape and
size necessary for flight. So while the general morphology
is similar, structure and organization of these wings greatly
vary [e.g., the bird wing is formed by the first three fingers
that support flight feathers (fingers 4–5 have been lost); the
bat wing is formed by a thin flexible skin stretched over the
fingers 2–5; the pterosaur wing is formed by skin and other
tissues attached to an elongated fourth finger and reinforced
with closely spaced fibers].
In contrast, parallel evolution is indicated when two
lineages originate from similar ancestral phenotypes and
evolve in the same trajectory towards a similar endpoint
(Fig. 3b; Revell et al. 2007). It is often assumed in parallel
evolution that the same genes underlying developmental
processes are involved in the morphological change in
separate lineages. Further, some argue that these changes
at the gene level might act to constrain the type of
morphological change that can occur (Wake 1991; Gould
2002). Until recently, it was extremely difficult to test
whether (or how) gene expression changed for most species
involved in putative parallelisms. For this reason, most
researchers apply a morphological definition of parallel
evolution that relies on pattern and can be more broadly
applied, rather than use a definition restricted by identification of similar genetic change.
Distinguishing between parallel and convergent evolution is important because each implies a pathway underlying the evolutionary change (character evolution). But are
these two evolutionary pathways mutually exclusive?
Convergent vs. Parallel Evolution
From the preceding discussion, it should be clear that a
myriad of eye types exists throughout the molluscs.
Additionally, the same eye types appear in distinct groups
of organisms. This brings up an interesting question: how
did they come to be? To answer this question requires
understanding the evolutionary processes that generated
them and the paths by which they have originated. This is
done by examining the patterns of convergent and parallel
evolution.
Convergence is the independent evolution of similar
structural or functional components in two or more
Fig. 3 Different evolutionary trajectories seen in convergent and
parallel evolution. a In convergent evolution, ancestral phenotypes (A0
and B0) are unalike but reach a similar endpoint in the descendent taxa
(A and B). b In parallel evolution, ancestral phenotypes (C0 and D0)
are similar and evolve in trajectories towards similar endpoints in the
descendents (C and D)
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Several authors have suggested a continuum between
parallelism and convergence (Gould 2002; Donoghue
2005), which may result in instances of partial homology
in an organ as a result of both convergence and parallel
processes (for example, see Sattler 1991; Baum and
Donoghue 2002). If this posit is true, it fits with the
concept of biological systems organization in hierarchic
levels (e.g., Vrba and Eldredge 1984). Just as an organism
is composed of different organs, organs are made from
tissue types, and tissue types are derived from specific cell
types, the eye can be decomposed into component parts.
Each of the levels or modules can have different histories
and separate evolutionary trajectories (see examples in Serb
and Oakley 2005) and therefore may exhibit either
convergent or parallel patterns.
What Can Molluscan Eyes Tell Us About Convergent
and Parallel Evolution?
For almost 140 years, the most cited example of convergent
evolution was the likeness between the camera-type eyes of
cephalopods and vertebrates (Darwin 1872; Packard 1972;
Futuyma 1998; Land and Nilsson 2002). However, the idea
that morphological similarity between cephalopod and
vertebrate eyes is a result of convergence has been
challenged by a growing number of researchers (Eakin
1979; Zuckerkandl 1994; Tomarev et al. 1997; Gould
2002). The strongest line of evidence against convergence
is the discovery of a conserved gene network, including the
gene Pax6 that governs eye organogenesis in vertebrate and
invertebrate lineages (Quiring et al. 1994). One might
suppose that if all animal eyes are regulated by the same
gene network, then eyes must also share a common origin
and that similarity between cephalopod and vertebrate eyes
evolved as a parallelism due to constraint in development
and not convergence. However, it is likely that the camera
eyes of cephalopods and vertebrates have degrees of both
convergent and parallel evolution. Eyes are not just single
irreducible entities, but can be viewed as containing different levels of biological complexity nested in a hierarchical fashion (e.g., Serb and Oakley 2005). The eye can be
subdivided into modules such as genetic networks (i.e.,
Pax6 network), photoreceptor cell types, crystallin proteins
that make up the lens, phototransduction pathways that
convert light into a chemical signal, and the eye itself as a
morphological structure. Therefore, convergence may occur
at one level, perhaps adult morphology of the eye, and
parallelism may take place at other levels, such as genetic
regulatory networks or photoreceptor cell types. Each
module can be tested for convergent or parallel patterns.
Until recently, it was difficult to rigorously test these
hypotheses. A new method developed by Revell et al.
445
(2007) distinguishes between convergence and parallelism
using phylogenetic methods. This method incorporates
morphological data on derived (extant) taxa and reconstructs the ancestral condition from the phylogeny. The
path of phenotypic evolution is expressed as the difference
between ancestor and descendant phenotypes for each
lineage. These vectors are graphed, and their directions are
compared to distinguish convergent and parallel patterns.
To accomplish these tests for cephalopod and vertebrate
eyes, robust phylogenetic hypotheses of the cephalopods
and the remaining Mollusca and the vertebrates within the
Chordata would first be required. In addition, data must be
generated from different eye modules for both molluscs and
chordates. Ancestral phenotypes would be estimated from
the extant taxa and the phylogeny. Changes in phenotypes
from ancestor to descendent would be compared (as vectors)
to other lineages at each level of biological complexity to
develop a more complete estimation of evolutionary pattern.
Eyes from other molluscan lineages also could be used
to study convergence and parallel patterns. For example,
the compound eye in ark clams and arthropods would be an
interesting comparison. Some work has been done on the
cellular structure of the compound eyes of ark clams
(Nilsson 1994; Nilsson Kelber 2007). However, nothing is
known about the ark clam eye below the cellular level.
Unlike the immense data on the compound eye of
Drosophila, we know little to nothing of the developmental
ontogeny, establishment of ommatidial patterning, or
genetic mechanisms in eye organogenesis of the ark clams.
Data from these modules will be necessary to test convergence and parallelism between molluscs and arthropods.
Other opportunities to study convergence or parallelism
in Mollusca occur within classes, such as Gastropoda. As
stated above, the eyes of gastropods range from simple eye
pits to complex lens eyes. Although gastropod eyes have
been used as a textbook example of Darwin’s (1859) eye
gradient to explain how an eye could evolve by natural
selection (Strickberger 1990; Ridley 2003), these eye types
have not been mapped on a phylogeny to formally test
these assertions. It is likely that gastropod eyes do not fit a
simple gradient of increasing complexity (see Fig. 1 in
Oakley and Pankey 2008) but are instead characterized by a
complex and interesting history involving multiple losses or
gains of eyes, with similarities due to convergent and/or
parallel evolution confounding those similarities due to
common ancestry. One interesting example that needs
further attention is the variation in retinal shape and optics
across pulmonate gastropods (Meyer-Rochow and Bobkova
2001; Gál et al. 2004). In conclusion, patterns in eye
evolution can only be properly evaluated as convergence
versus parallelism by developing robust phylogenies paired
with comparative studies of eye morphology across specific
groups.
446
Summary
Molluscs provide multiple opportunities to study the eye
and general evolutionary processes. The incredible amount
of phenotypic variation in molluscan eyes has been
woefully underutilized by both evolutionary biologists and
eye researchers. Future work on molluscs should include
developing molluscan models to study ontogenetic progression (Serb 2008), expanding the knowledge of subcellular
processes such as genomics and genetic regulation networks, and generating comprehensive phylogenetic hypotheses to identify patterns of convergence and parallelism.
Acknowledgments We are grateful to T. Ryan Gregory for inviting
us to participate in this special issue on eyes. Dustine Pruszko
prepared the drawings in Fig. 1. We thank Kevin Roe, Autum Pairett,
and Jill Hansen for comments on an earlier draft and Dean Adams and
Nicole Valenzuela for insightful discussion. D.J.E. thanks Andrea
Macaluso, Springer Office of Publication, for encouragement to attend
the American Malacological Society 2007 symposium organized by J.
M.S. on molluscan eye evolution in Antwerp, Belgium where this
review article originated. This work is supported by a grant from the
National Science Foundation (DEB-0614153) to J.M.S.
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